Identification of quantitative trait loci associated with R1-mediated resistance to powdery mildew and sex determination in hop (Humulus lupulus L.)

Joshua S. Havill; Briana J. Richardson; Charlie L. Rohwer; David H. Gent; John A. Henning; Gary J. Muehlbauer

doi:10.1007/s00122-023-04399-7

Identification of quantitative trait loci associated with R1-mediated resistance to powdery mildew and sex determination in hop (Humulus lupulus L.)

Joshua S. Havill, Briana J. Richardson, Charlie L. Rohwer, David H. Gent, John A. Henning, Gary J. Muehlbauer

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Abstract

Key message: Two QTL were identified using linkage mapping approaches, one on hop linkage group 3 (qHl_Chr3.PMR1) associated with powdery mildew resistance and a second on linkage group 10 (cqHl_ChrX.SDR1) associated with sex determination. Abstract: Hop (Humulus lupulus L.) is a dioecious species cultivated for use in beer. Hop powdery mildew, caused by Podosphaera macularis, is a constraint in many growing regions. Thus, identifying markers associated with powdery mildew resistance and sex provides the opportunity to pyramid R-genes and select female plants as seedlings, respectively. Our objectives were to characterize the genetic basis of R1-mediated resistance in the cultivar Zenith which provides resistance to pathogen races in the US, identify quantitative trait loci (QTL) associated with R1 and sex, and develop markers for molecular breeding-based approaches. Phenotypic evaluation of the population indicated that R1-based resistance and sex are inherited monogenically. We constructed a genetic map using 1339 single nucleotide polymorphisms (SNPs) based upon genotype-by-sequencing of 128 F₁ progeny derived from a Zenith × USDA 21058M biparental population. SNPs were assigned to 10 linkage groups comprising a map length of 1204.97 cM with an average density of 0.94 cM/marker. Quantitative trait locus mapping identified qHl_Chr3.PMR1, associated with R1 on linkage group 3 (LOD = 23.57, R ² = 57.2%), and cqHl_ChrX.SDR1, associated with sex on linkage group 10 (LOD = 5.42, R ² = 25.0%). Kompetitive allele-specific PCR (KASP) assays were developed for both QTL and assessed against diverse germplasm. Our results indicate that KASP markers associated with R1 may be limited to materials that are pedigree-related to Zenith, whereas markers associated with sex may be transferable across populations. The high-density map, QTL, and associated KASP markers will enable selecting for sex and R1-mediated resistance in hop.

Original language	English (US)
Article number	154
Journal	Theoretical and Applied Genetics
Volume	136
Issue number	7
DOIs	https://doi.org/10.1007/s00122-023-04399-7
State	Published - Jul 2023

Bibliographical note

Funding Information:
The authors express their gratitude to Adam Schrankler, Cristiane Tayumi-Taniguti, Antonio Augusto Franco Garcia, and John Lovell for their technical assistance and feedback. The authors also thank Sarah Carey, Alex Harkess, Kayla Altendorf, Matthew Clark, Ben Mansfeld, and Jonathan Fresnedo-Ramirez for their discussions with genetic mapping, QTL identification and overlap, and KASP marker design. The authors acknowledge the Hop Research Institute in Czech Republic and the National Clonal Germplasm Repository in Corvallis, OR for providing germplasm samples for use in KASP assays. The authors acknowledge the Minnesota Supercomputing Institute (MSI) at the University of Minnesota for providing resources that contributed to the research results reported within this paper.

Funding Information:
This work was supported by funding from the Minnesota Department of Agriculture, the Brewers Association, and Hopsteiner, S. S. Steiner, Inc. JSH was also supported by fellowships from the Plant and Microbial Biology graduate program and the Department of Agronomy and Plant Genetics at the University of Minnesota.

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© 2023, The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.

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@article{52b973df7a8d4f7aa6da6979dbf0b3cd,

title = "Identification of quantitative trait loci associated with R1-mediated resistance to powdery mildew and sex determination in hop (Humulus lupulus L.)",

abstract = "Key message: Two QTL were identified using linkage mapping approaches, one on hop linkage group 3 (qHl_Chr3.PMR1) associated with powdery mildew resistance and a second on linkage group 10 (cqHl_ChrX.SDR1) associated with sex determination. Abstract: Hop (Humulus lupulus L.) is a dioecious species cultivated for use in beer. Hop powdery mildew, caused by Podosphaera macularis, is a constraint in many growing regions. Thus, identifying markers associated with powdery mildew resistance and sex provides the opportunity to pyramid R-genes and select female plants as seedlings, respectively. Our objectives were to characterize the genetic basis of R1-mediated resistance in the cultivar Zenith which provides resistance to pathogen races in the US, identify quantitative trait loci (QTL) associated with R1 and sex, and develop markers for molecular breeding-based approaches. Phenotypic evaluation of the population indicated that R1-based resistance and sex are inherited monogenically. We constructed a genetic map using 1339 single nucleotide polymorphisms (SNPs) based upon genotype-by-sequencing of 128 F1 progeny derived from a Zenith × USDA 21058M biparental population. SNPs were assigned to 10 linkage groups comprising a map length of 1204.97 cM with an average density of 0.94 cM/marker. Quantitative trait locus mapping identified qHl_Chr3.PMR1, associated with R1 on linkage group 3 (LOD = 23.57, R 2 = 57.2%), and cqHl_ChrX.SDR1, associated with sex on linkage group 10 (LOD = 5.42, R 2 = 25.0%). Kompetitive allele-specific PCR (KASP) assays were developed for both QTL and assessed against diverse germplasm. Our results indicate that KASP markers associated with R1 may be limited to materials that are pedigree-related to Zenith, whereas markers associated with sex may be transferable across populations. The high-density map, QTL, and associated KASP markers will enable selecting for sex and R1-mediated resistance in hop.",

author = "Havill, {Joshua S.} and Richardson, {Briana J.} and Rohwer, {Charlie L.} and Gent, {David H.} and Henning, {John A.} and Muehlbauer, {Gary J.}",

note = "Funding Information: The authors express their gratitude to Adam Schrankler, Cristiane Tayumi-Taniguti, Antonio Augusto Franco Garcia, and John Lovell for their technical assistance and feedback. The authors also thank Sarah Carey, Alex Harkess, Kayla Altendorf, Matthew Clark, Ben Mansfeld, and Jonathan Fresnedo-Ramirez for their discussions with genetic mapping, QTL identification and overlap, and KASP marker design. The authors acknowledge the Hop Research Institute in Czech Republic and the National Clonal Germplasm Repository in Corvallis, OR for providing germplasm samples for use in KASP assays. The authors acknowledge the Minnesota Supercomputing Institute (MSI) at the University of Minnesota for providing resources that contributed to the research results reported within this paper. Funding Information: This work was supported by funding from the Minnesota Department of Agriculture, the Brewers Association, and Hopsteiner, S. S. Steiner, Inc. JSH was also supported by fellowships from the Plant and Microbial Biology graduate program and the Department of Agronomy and Plant Genetics at the University of Minnesota. Publisher Copyright: {\textcopyright} 2023, The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.",

year = "2023",

month = jul,

doi = "10.1007/s00122-023-04399-7",

language = "English (US)",

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journal = "Theoretical and Applied Genetics",

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T1 - Identification of quantitative trait loci associated with R1-mediated resistance to powdery mildew and sex determination in hop (Humulus lupulus L.)

AU - Havill, Joshua S.

AU - Richardson, Briana J.

AU - Rohwer, Charlie L.

AU - Gent, David H.

AU - Henning, John A.

AU - Muehlbauer, Gary J.

N1 - Funding Information: The authors express their gratitude to Adam Schrankler, Cristiane Tayumi-Taniguti, Antonio Augusto Franco Garcia, and John Lovell for their technical assistance and feedback. The authors also thank Sarah Carey, Alex Harkess, Kayla Altendorf, Matthew Clark, Ben Mansfeld, and Jonathan Fresnedo-Ramirez for their discussions with genetic mapping, QTL identification and overlap, and KASP marker design. The authors acknowledge the Hop Research Institute in Czech Republic and the National Clonal Germplasm Repository in Corvallis, OR for providing germplasm samples for use in KASP assays. The authors acknowledge the Minnesota Supercomputing Institute (MSI) at the University of Minnesota for providing resources that contributed to the research results reported within this paper. Funding Information: This work was supported by funding from the Minnesota Department of Agriculture, the Brewers Association, and Hopsteiner, S. S. Steiner, Inc. JSH was also supported by fellowships from the Plant and Microbial Biology graduate program and the Department of Agronomy and Plant Genetics at the University of Minnesota. Publisher Copyright: © 2023, The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.

PY - 2023/7

Y1 - 2023/7

N2 - Key message: Two QTL were identified using linkage mapping approaches, one on hop linkage group 3 (qHl_Chr3.PMR1) associated with powdery mildew resistance and a second on linkage group 10 (cqHl_ChrX.SDR1) associated with sex determination. Abstract: Hop (Humulus lupulus L.) is a dioecious species cultivated for use in beer. Hop powdery mildew, caused by Podosphaera macularis, is a constraint in many growing regions. Thus, identifying markers associated with powdery mildew resistance and sex provides the opportunity to pyramid R-genes and select female plants as seedlings, respectively. Our objectives were to characterize the genetic basis of R1-mediated resistance in the cultivar Zenith which provides resistance to pathogen races in the US, identify quantitative trait loci (QTL) associated with R1 and sex, and develop markers for molecular breeding-based approaches. Phenotypic evaluation of the population indicated that R1-based resistance and sex are inherited monogenically. We constructed a genetic map using 1339 single nucleotide polymorphisms (SNPs) based upon genotype-by-sequencing of 128 F1 progeny derived from a Zenith × USDA 21058M biparental population. SNPs were assigned to 10 linkage groups comprising a map length of 1204.97 cM with an average density of 0.94 cM/marker. Quantitative trait locus mapping identified qHl_Chr3.PMR1, associated with R1 on linkage group 3 (LOD = 23.57, R 2 = 57.2%), and cqHl_ChrX.SDR1, associated with sex on linkage group 10 (LOD = 5.42, R 2 = 25.0%). Kompetitive allele-specific PCR (KASP) assays were developed for both QTL and assessed against diverse germplasm. Our results indicate that KASP markers associated with R1 may be limited to materials that are pedigree-related to Zenith, whereas markers associated with sex may be transferable across populations. The high-density map, QTL, and associated KASP markers will enable selecting for sex and R1-mediated resistance in hop.

AB - Key message: Two QTL were identified using linkage mapping approaches, one on hop linkage group 3 (qHl_Chr3.PMR1) associated with powdery mildew resistance and a second on linkage group 10 (cqHl_ChrX.SDR1) associated with sex determination. Abstract: Hop (Humulus lupulus L.) is a dioecious species cultivated for use in beer. Hop powdery mildew, caused by Podosphaera macularis, is a constraint in many growing regions. Thus, identifying markers associated with powdery mildew resistance and sex provides the opportunity to pyramid R-genes and select female plants as seedlings, respectively. Our objectives were to characterize the genetic basis of R1-mediated resistance in the cultivar Zenith which provides resistance to pathogen races in the US, identify quantitative trait loci (QTL) associated with R1 and sex, and develop markers for molecular breeding-based approaches. Phenotypic evaluation of the population indicated that R1-based resistance and sex are inherited monogenically. We constructed a genetic map using 1339 single nucleotide polymorphisms (SNPs) based upon genotype-by-sequencing of 128 F1 progeny derived from a Zenith × USDA 21058M biparental population. SNPs were assigned to 10 linkage groups comprising a map length of 1204.97 cM with an average density of 0.94 cM/marker. Quantitative trait locus mapping identified qHl_Chr3.PMR1, associated with R1 on linkage group 3 (LOD = 23.57, R 2 = 57.2%), and cqHl_ChrX.SDR1, associated with sex on linkage group 10 (LOD = 5.42, R 2 = 25.0%). Kompetitive allele-specific PCR (KASP) assays were developed for both QTL and assessed against diverse germplasm. Our results indicate that KASP markers associated with R1 may be limited to materials that are pedigree-related to Zenith, whereas markers associated with sex may be transferable across populations. The high-density map, QTL, and associated KASP markers will enable selecting for sex and R1-mediated resistance in hop.

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Identification of quantitative trait loci associated with R1-mediated resistance to powdery mildew and sex determination in hop (Humulus lupulus L.)

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